Repeatability in lactation performance and the consequences for maternal reproductive success in gray seals

Abstract

In mammals, the most significant maternal effect on offspring growth during lactation is the ability of females to efficiently transfer milk energy to their neonates. However, despite the importance of the transfer of milk energy to both maternal and offspring fitness, nothing is known about the extent to which variation among females may be attributed to differences in individual quality or environmental variation in natural populations. We measured repeatability over multiple lactation periods in components of lactation performance in free-ranging, multiparous gray seal (Halichoerus grypus) females to examine to what extent variation among females in pup weaning mass may be attributed to inherent differences in their physiological capacity to deliver milk energy. Levels of repeatability were high for milk composition (r = 0.38-0.50), daily milk output (r = 0.46), and the duration of lactation (r = 0.57), demonstrating that there are consistent differences among females in these characters across lactations and that the overall capacity of gray seal females to deliver milk energy to their pups is characteristic of individuals. The repeatability in pup weaning mass (r = 0.48) was consistent with the values for the components of total milk energy output and suggests that, over a large proportion of their reproductive life, individual gray seal females will consistently wean pups with greater or lesser probabilities of survival. Our results suggest that inherent differences among females in their physiological capacity to deliver milk energy may be an important component of variation in individual quality and, thus, lifetime reproductive success in mammals. High levels of repeatability also suggest that components of milk energy transfer may have a significant heritable genetic basis.

Primiparous and multiparous females differ in mammary gland alveolar development: implications for milk production

“…The values for milk composition (Table1), estimated daily milk output and the relative growth of pups over lactation (Table2) were consistent with previous observations for primiparous and multiparous grey seal females (Lang et al, 2009;Lang et al, 2011a). These results indicate that the transfer of milk energy to pups was not significantly affected following the biopsy procedures at either early or peak lactation and that the females selected for this study were representative of the population.…”

“…To ensure that the values for the females selected for this study were consistent with our previous observations for multiparous and primiparous females (Lang et al, 2009;Lang et al, 2011a) and to verify that our biopsy procedure did not adversely affect mammary gland function, we compared milk composition, daily milk output and pup growth patterns between the groups. Because changes in these characters with lactation stage have already been well characterized for this species (Iverson et al, 1993;Mellish et al, 1999a, Lang et al, 2009 P<0.001). Pup growth followed the same pattern in both groups throughout lactation.…”

“…In grey seals, milk fat increases from parturition until reaching peak values at approximately day 8 postpartum and then remains relatively stable over the remainder of lactation (Iverson et al, 1993). To account for the non-linear change in milk fat content over the measurement period, we calculated a weighted harmonic mean for a female's percent milk fat (see Lang et al, 2009). Following an initial decline shortly after parturition, milk protein content remains relatively constant throughout the remainder of lactation in grey seals (Iverson et al, 1993) and, therefore, early and peak lactation values were averaged.…”

“…However, females may vary in their ability to deliver milk energy to their offspring independent of variation in factors such as resource availability, levels of body energy stores or body size (e.g. Yang et al, 1989;Lang et al, 2009) as a consequence of differences in the capacity of their mammary glands for milk production (Knight, 2000). Thus, identifying sources of variation in mammary gland capacity is important to our understanding of variation in reproductive success both among and within individuals.…”

Dynamic Influence of Maternal and Pup Traits on Maternal Care during Lactation in an Income Breeder, the Antarctic Fur Seal

“…Another potential weakness of this study is that because of logistical constraints, we used mean milk water and energy content values that were averaged from all milk samples collected during the respective study periods. Individual females may differ in the composition of their milk because of their physiological capacity to produce milk and/or because of dietary differences, and this might affect some of the results in the study (Lea et al 2006;McDonald and Crocker 2006;Lang et al 2009). …”